Antitumor effect of afatinib, as a human epidermal growth factor receptor 2-targeted therapy, in lung cancers harboring HER2 oncogene alterations

Cancer Science

Volumn 107, Issue 1, 2016, Pages 45-52

  Suzawa, Ken ^a   Toyooka, Shinichi ^a   Sakaguchi, Masakiyo ^a   Morita, Mizuki ^a   Yamamoto, Hiromasa ^a   Tomida, Shuta ^a   Ohtsuka, Tomoaki ^a   Watanabe, Mototsugu ^a   Hashida, Shinsuke ^a   Maki, Yuho ^a   Soh, Junichi ^a   Asano, Hiroaki ^a   Tsukuda, Kazunori ^a   Miyoshi, Shinichiro ^a  

^a OKAYAMA UNIVERSITY   (Japan)

Author keywords

Afatinib; ERBB2; HER2; HER2 targeted therapy; Non small cell lung cancer

Indexed keywords

AFATINIB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GEFITINIB; ANTINEOPLASTIC AGENT; ERBB2 PROTEIN, HUMAN; QUINAZOLINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; BRONCHUS MUCOSA; CELL CYCLE G1 PHASE; CELL DEATH; CELL LINE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; DRUG EFFICACY; DRUG SENSITIVITY; EPITHELIUM CELL; FEMALE; GENE AMPLIFICATION; GENE MUTATION; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG CANCER; MOUSE; MUTANT; NON SMALL CELL LUNG CANCER; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; TUMOR XENOGRAFT; WILD TYPE; ANIMAL; DRUG SCREENING; GENETIC TRANSFECTION; GENETICS; LUNG TUMOR; NONOBESE DIABETIC MOUSE; PATHOLOGY; PROTO ONCOGENE; REAL TIME POLYMERASE CHAIN REACTION; SCID MOUSE; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; FEMALE; GENES, ERBB-2; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED NOD; MICE, SCID; QUINAZOLINES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, ERBB-2; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84956728134     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12845     Document Type: Article

References (42)

1. Youlden DR, Cramb SM, Baade PD. The International Epidemiology of Lung Cancer: geographical distribution and secular trends. J Thorac Oncol 2008; 3: 819-31.
2. Mok TS, Wu YL, Thongprasert S et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009; 361: 947-57.
3. Kwak EL, Bang YJ, Camidge DR et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 2010; 363: 1693-703.
4. Kris MG, Johnson BE, Berry LD et al. Using multiplexed assays of oncogenic drivers in lung cancers to select targeted drugs. JAMA 2014; 311: 1998-2006.
5. Pao W, Girard N. New driver mutations in non-small-cell lung cancer. Lancet Oncol 2011; 12: 175-80.
6. Chazin VR, Kaleko M, Miller AD, Slamon DJ. Transformation mediated by the human HER-2 gene independent of the epidermal growth factor receptor. Oncogene 1992; 7: 1859-66.
7. Neve RM, Lane HA, Hynes NE. The role of overexpressed HER2 in transformation. Ann Oncol 2001; 12(Suppl 1): S9-13.
8. Wang SE, Narasanna A, Perez-Torres M et al. HER2 kinase domain mutation results in constitutive phosphorylation and activation of HER2 and EGFR and resistance to EGFR tyrosine kinase inhibitors. Cancer Cell 2006; 10: 25-38.
9. Perera SA, Li D, Shimamura T et al. HER2YVMA drives rapid development of adenosquamous lung tumors in mice that are sensitive to BIBW2992 and rapamycin combination therapy. Proc Natl Acad Sci U S A 2009; 106: 474-9.
10. Tan D, Deeb G, Wang J et al. HER-2/neu protein expression and gene alteration in stage I-IIIA non-small-cell lung cancer: a study of 140 cases using a combination of high throughput tissue microarray, immunohistochemistry, and fluorescent in situ hybridization. Diagn Mol Pathol 2003; 12: 201-11.
11. Pellegrini C, Falleni M, Marchetti A et al. HER-2/Neu alterations in non-small cell lung cancer: a comprehensive evaluation by real time reverse transcription-PCR, fluorescence in situ hybridization, and immunohistochemistry. Clin Cancer Res 2003; 9: 3645-52.
12. Cappuzzo F, Varella-Garcia M, Shigematsu H et al. Increased HER2 gene copy number is associated with response to gefitinib therapy in epidermal growth factor receptor-positive non-small-cell lung cancer patients. J Clin Oncol 2005; 23: 5007-18.
13. Swanton C, Futreal A, Eisen T. Her2-targeted therapies in non-small cell lung cancer. Clin Cancer Res 2006; 12: 4377s-83s.
14. Stephens P, Hunter C, Bignell G et al. Lung cancer: intragenic ERBB2 kinase mutations in tumours. Nature 2004; 431: 525-6.
15. Shigematsu H, Takahashi T, Nomura M et al. Somatic mutations of the HER2 kinase domain in lung adenocarcinomas. Cancer Res 2005; 65: 1642-6.
16. Yamamoto H, Higasa K, Sakaguchi M et al. Novel germline mutation in the transmembrane domain of HER2 in familial lung adenocarcinomas. J Natl Cancer Inst 2014; 106: djt338.
17. Sequist LV, Yang JC, Yamamoto N et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J Clin Oncol 2013; 31: 3327-34.
18. Wu YL, Zhou C, Hu CP et al. Afatinib versus cisplatin plus gemcitabine for first-line treatment of Asian patients with advanced non-small-cell lung cancer harbouring EGFR mutations (LUX-Lung 6): an open-label, randomised phase 3 trial. Lancet Oncol 2014; 15: 213-22.
19. Gandhi J, Zhang J, Xie Y et al. Alterations in genes of the EGFR signaling pathway and their relationship to EGFR tyrosine kinase inhibitor sensitivity in lung cancer cell lines. PLoS ONE 2009; 4: e4576.
20. Girard L, Zochbauer-Muller S, Virmani AK, Gazdar AF, Minna JD. Genome-wide allelotyping of lung cancer identifies new regions of allelic loss, differences between small cell lung cancer and non-small cell lung cancer, and loci clustering. Cancer Res 2000; 60: 4894-906.
21. Sakaguchi M, Watanabe M, Kinoshita R et al. Dramatic increase in expression of a transgene by insertion of promoters downstream of the cargo gene. Mol Biotechnol 2014; 56: 621-30.
22. Frishman D, Argos P. Knowledge-based protein secondary structure assignment. Proteins 1995; 23: 566-79.
23. Soh J, Okumura N, Lockwood WW et al. Oncogene mutations, copy number gains and mutant allele specific imbalance (MASI) frequently occur together in tumor cells. PLoS ONE 2009; 4: e7464.
24. Shien K, Toyooka S, Yamamoto H et al. Acquired resistance to EGFR inhibitors is associated with a manifestation of stem cell-like properties in cancer cells. Cancer Res 2013; 73: 3051-61.
25. Kubo T, Yamamoto H, Lockwood WW et al. MET gene amplification or EGFR mutation activate MET in lung cancers untreated with EGFR tyrosine kinase inhibitors. Int J Cancer 2009; 124: 1778-84.
26. Engelman JA, Janne PA, Mermel C et al. ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinib-sensitive non-small cell lung cancer cell lines. Proc Natl Acad Sci U S A 2005; 102: 3788-93.
27. Li D, Ambrogio L, Shimamura T et al. BIBW2992, an irreversible EGFR/HER2 inhibitor highly effective in preclinical lung cancer models. Oncogene 2008; 27: 4702-11.
28. Slamon DJ, Leyland-Jones B, Shak S et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 2001; 344: 783-92.
29. Bang YJ, Van Cutsem E, Feyereislova A et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 2010; 376: 687-97.
30. Gatzemeier U, Groth G, Butts C et al. Randomized phase II trial of gemcitabine-cisplatin with or without trastuzumab in HER2-positive non-small-cell lung cancer. Ann Oncol 2004; 15: 19-27.
31. Lara PN Jr, Laptalo L, Longmate J et al. Trastuzumab plus docetaxel in HER2/neu-positive non-small-cell lung cancer: a California Cancer Consortium screening and phase II trial. Clin Lung Cancer 2004; 5: 231-6.
32. Clamon G, Herndon J, Kern J et al. Lack of trastuzumab activity in nonsmall cell lung carcinoma with overexpression of erb-B2: 39810: a phase II trial of Cancer and Leukemia Group B. Cancer 2005; 103: 1670-5.
33. De Greve J, Teugels E, Geers C et al. Clinical activity of afatinib (BIBW 2992) in patients with lung adenocarcinoma with mutations in the kinase domain of HER2/neu. Lung Cancer 2012; 76: 123-7.
34. Mazieres J, Peters S, Lepage B et al. Lung cancer that harbors an HER2 mutation: epidemiologic characteristics and therapeutic perspectives. J Clin Oncol 2013; 31: 1997-2003.
35. Shimamura T, Ji H, Minami Y et al. Non-small-cell lung cancer and Ba/F3 transformed cells harboring the ERBB2 G776insV_G/C mutation are sensitive to the dual-specific epidermal growth factor receptor and ERBB2 inhibitor HKI-272. Cancer Res 2006; 66: 6487-91.
36. Minami Y, Shimamura T, Shah K et al. The major lung cancer-derived mutants of ERBB2 are oncogenic and are associated with sensitivity to the irreversible EGFR/ERBB2 inhibitor HKI-272. Oncogene 2007; 26: 5023-7.
37. Engelman JA, Zejnullahu K, Gale CM et al. PF00299804, an irreversible pan-ERBB inhibitor, is effective in lung cancer models with EGFR and ERBB2 mutations that are resistant to gefitinib. Cancer Res 2007; 67: 11924-32.
38. Murakami H, Tamura T, Takahashi T et al. Phase I study of continuous afatinib (BIBW 2992) in patients with advanced non-small cell lung cancer after prior chemotherapy/erlotinib/gefitinib (LUX-Lung 4). Cancer Chemother Pharmacol 2012; 69: 891-9.
39. Arcila ME, Chaft JE, Nafa K et al. Prevalence, clinicopathologic associations, and molecular spectrum of ERBB2 (HER2) tyrosine kinase mutations in lung adenocarcinomas. Clin Cancer Res 2012; 18: 4910-8.
40. Kobayashi S, Boggon TJ, Dayaram T et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 2005; 352: 786-92.
41. Balak MN, Gong Y, Riely GJ et al. Novel D761Y and common secondary T790M mutations in epidermal growth factor receptor-mutant lung adenocarcinomas with acquired resistance to kinase inhibitors. Clin Cancer Res 2006; 12: 6494-501.
42. Takezawa K, Pirazzoli V, Arcila ME et al. HER2 amplification: a potential mechanism of acquired resistance to EGFR inhibition in EGFR-mutant lung cancers that lack the second-site EGFR T790M mutation. Cancer Discov 2012; 2: 922-33.